Effects of the donor-acceptor distance and dynamics on hydride tunneling in the dihydrofolate reductase catalyzed reaction

Journal of the American Chemical Society

Volumn 134, Issue 3, 2012, Pages 1738-1745

  Stojković, Vanja ^a   Perissinotti, Laura L ^a   Willmer, Daniel ^a   Benkovic, Stephen J ^b   Kohen, Amnon ^a  

^a E11 SSH   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION PARAMETER; ACTIVE SITE; CATALYZED REACTIONS; CLASSICAL MOLECULAR DYNAMICS; DIHYDROFOLATE REDUCTASE; DONOR-ACCEPTOR DISTANCE; E. COLI; ENZYME CATALYZED REACTION; HYDROPHOBIC RESIDUES; INTRINSIC KINETICS; MD SIMULATION; PROTEIN DYNAMICS; SIDE-CHAINS; STRUCTURE-FUNCTION CORRELATION; TEMPERATURE DEPENDENCE; THERMALLY ACTIVATED; TRANSFER REACTION; WILD-TYPE ENZYMES;

CATALYSIS; DYNAMICS; ENZYMES; ESCHERICHIA COLI; HYDROGEN; HYDROPHOBICITY; ISOTOPES; MOLECULAR DYNAMICS; REACTION KINETICS; TEMPERATURE DISTRIBUTION;

HYDRIDES;

DIHYDROFOLATE REDUCTASE;

ARTICLE; CATALYSIS; DONOR ACCEPTOR DISTANCE; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME KINETICS; ENZYME STRUCTURE; HYDROPHOBIC INTERACTION CHROMATOGRAPHY; MOLECULAR DYNAMICS; SIMULATION; TEMPERATURE; WILD TYPE;

CATALYTIC DOMAIN; ESCHERICHIA COLI; KINETICS; MODELS, MOLECULAR; MUTATION; TETRAHYDROFOLATE DEHYDROGENASE;

EID: 84856247363     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/ja209425w     Document Type: Article

References (67)

1. Pauling, L. Nature 1948, 161, 707-709
2. Kohen, A. In Isotope effects in chemistry and biology; Kohen, A.; Limbach, H. H., Eds.; Taylor & Francis, CRC Press: Boca Raton, FL, 2006; Vol. Ch. 28, pp 743-764.
3. Schwartz, S. D. In Isotope effects in chemistry and biology; Kohen, A.; Limbach, H. H., Eds.; Taylor & Francis, CRC Press: Boca Raton, FL, 2006; Vol. Ch. 18, pp 475-498.
4. Truhlar, D. G. In Isotope effects in chemistry and biology; Kohen, A.; Limbach, H. H., Eds.; Taylor & Francis, CRC Press: Boca Raton, FL, 2006; Vol. Ch. 22, pp 579-620.
5. Warshel, A.; Olsson, M. H. M.; Villa-Freixa, J. In Isotope effects in chemistry and biology; Kohen, A.; Limbach, H. H., Eds.; Taylor & Francis, CRC Press: Boca Raton, FL, 2006, pp 621-644.
6. Kiefer, P. M.; Hynes, J. T. In Isotope effects in chemistry and biology; Kohen, A.; Limbach, H. H., Eds.; Taylor & Francis, CRC Press: Boca Raton, FL, 2006; Vol. Ch. 21, pp 549-578.
7. Sutcliffe, M. J.; Masgrau, L.; Roujeinikova, A.; Johannissen, L. O.; Hothi, P.; Basran, J.; Ranaghan, K. E.; Mulholland, A. J.; Leys, D.; Scrutton, N. S. Philos. Trans. R. Soc., B 2006, 361, 1375-1386
8. Fan, F.; Gadda, G. J. Am. Chem. Soc. 2005, 127, 17954-17961
9. Boehr, D. D.; McElheny, D.; Dyson, H. J.; Wright, P. E. Science 2006, 313, 1638-1642
10. Hammes-Schiffer, S. In Quantum Tunnelling in Enzyme-Catalysed Reactions; Allemann, R. K.; Scrutton, N. S., Eds.; Royal Society of Chemistry: Cambridge, 2009; pp 79-104.
11. Nagel, Z. D.; Klinman, J. P. Chem. Rev. 2010, 110, PR41-67
12. Pudney, C. R.; Johannissen, L. O.; Sutcliffe, M. J.; Hay, S.; Scrutton, N. S. J. Am. Chem. Soc. 2010, 132, 11329-11335
13. Nagel, Z. D.; Dong, M.; Bahnson, B. J.; Klinman, J. P. Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 10520-10525
14. Hay, S.; Sutcliffe, M. J.; Scrutton, N. S. In Quantum Tunnelling in Enzyme-Catalysed Reactions; Scrutton, N. S.; Allemann, R. K., Eds.; RSC Publishing: 2009; pp 199-218.
15. Bandaria, J. N.; Dutta, S.; Nydegger, M. W.; Rock, W.; Kohen, A.; Cheatum, C. M. Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 17974-17979
16. Marcus, R. A.; Sutin, N. Biochem. Biophys. Acta 1985, 811, 265-322
17. Marcus, R. A. J. Phys. Chem. B 2007, 111, 6643-6654
18. Francisco, W. A.; Knapp, M. J.; Blackburn, N. J.; Klinman, J. P. J. Am. Chem. Soc. 2002, 124, 8194-8195
19. Antoniou, D.; Caratzoulas, S.; Kalyanaraman, C.; Mincer, J. S.; Schwartz, S. D. Eur. J. Biochem. 2002, 269, 3103-3112
20. Sutcliffe, M. J.; Scrutton, N. S. Eur. J. Biochem. 2002, 13, 3096-3102
21. Villa, J.; Warshel, A. J. Phys. Chem B 2001, 105, 7887-7907
22. Roston, D.; Kohen, A. Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 9572-9577
23. Hammes-Schiffer, S. Acc. Chem. Res. 2006, 39, 93-100
24. e + 2 × 1.04 Å. Also, when the DHA angle is fixed (on the reaction's time scale), then both DADs' fluctuations are coherent
25. Wang, Z.; Kohen, A. J. Am. Chem. Soc. 2010, 132, 9820-9825
26. Wang, L.; Goodey, N. M.; Benkovic, S. J.; Kohen, A. Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 15753-15758
27. Antoniou, D.; Schwartz, S. D. J. Phys. Chem. B 2001, 105, 5553-5558
28. Knapp, M. J.; Klinman, J. P. J. Am. Chem. Soc. 2002, 124, 3865-3874
29. Meyer, M. J.; Tomchick, D. R.; Klinman, J. P. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 1146-1151
30. Hay, S.; Scrutton, N. S. Biochemistry 2008, 47, 9880-9887
31. McCusker, K. P.; Klinman, J. P. J. Am. Chem. Soc. 2010, 132, 5114-5120
32. Bahnson, B. J.; Colby, T. D.; Chin, J. K.; Goldstein, B. M.; Klinman, J. P. Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 12797-12802
33. Colby, T. D.; Bahnson, B. J.; Chin, J. K.; Klinman, J. P.; Goldstein, B. M. Biochemistry 1998, 37, 9295-9304
34. Pudney, C. R.; McGrory, T.; Lafite, P.; Pang, J.; Hay, S.; Sutcliffe, M. J.; Scrutton, N. S. ChemBioChem 2009, 10, 1379-1384
35. Fierke, C. A.; Johnson, K. A.; Benkovic, S. J. Biochemistry 1987, 26, 4085-4092
36. Fierke, C. A.; Benkovic, S. J. Biochemistry 1989, 28, 478-486
37. Sikorski, R. S.; Wang, L.; Markham, K. A.; Rajagopalan, P. T. R.; Benkovic, S. J.; Kohen, A. J. Am. Chem. Soc. 2004, 126, 4778-4779
38. Wang, L.; Goodey, N. M.; Benkovic, S. J.; Kohen, A. Phil. Trans. R. Soc., B 2006, 361, 1307-1315
39. Wang, L.; Tharp, S.; Selzer, T.; Benkovic, S. J.; Kohen, A. Biochemistry 2006, 45, 1383-1392
40. Radkiewicz, J.; Brooks, C. J. Am. Chem. Soc. 2000, 122, 225-231
41. Wong, K. F.; Selzer, T.; Benkovic, S. J.; Hammes-Schiffer, S. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 6807-6812
42. Schnell, J. R.; Dyson, H. J.; Wright, P. E. Biochemistry 2004, 43, 374-383
43. Arora, K.; Brooks, C. L. I. J. Am. Chem. Soc. 2009, 131, 5642-5647
44. Adams, J. A.; Fierke, C. A.; Benkovic, S. J. Biochemistry 1991, 30, 11046-11054
45. Stojkovic, V.; Perissinoti, L. L.; Lee, J.; Benkovic, S.; Kohen, A. Chem. Commun. 2010, 46, 8974-8976
46. Markham, K. A.; Sikorski, R. S.; Kohen, A. Anal. Biochem. 2004, 325, 62-67
47. McCracken, J. A.; Wang, L.; Kohen, A. Anal. Biochem. 2003, 324, 131-136
48. Northrop, D. B. In Enzyme mechanism from isotope effects; Cook, P. F., Ed.; CRC Press: Boca Raton, FL, 1991; pp 181-202.
49. Case, D. A.; University of California: San Francisco, 2006.
50. Pearlman, D. A.; Case, D. A.; Caldwell, J. W.; Ross, W. S.; Cheatham, T. E., III; DeBolt, S.; Ferguson, D.; Seibel, G.; Kollman, P. A. Comput. Phys. Commun. 1995, 91, 1-41
51. Cheatham, T. E.; Cieplak, P.; Kollman, P. A. J. Biomol. Struct. Dyn. 1999, 16, 845-862
52. Walker, R. C.; De Souza, M. M.; Mercer, I. P.; Gould, I. R.; Klug, D. R. J. Phys. Chem. B 2002, 106, 11658-11665
53. Wang, J.; Wolf, R. M.; Caldwell, J. W.; Kollamn, P. A.; Case, D. A. J. Comput. Chem. 2004, 25, 1157-1174
54. Wang, J.; Cieplak, P.; Kollman, P. A. J. Comput. Chem. 2000, 21, 1049-1074
55. Wojdyr, M. J. Appl. Crystallogr. 2010, 43, 1126-1128
56. Creighton, T. E. Proteins. Structure and Molecular Principles; Freeman: New York, 1984.
57. Andrews, J.; Fierke, C. A.; Birdsall, B.; Ostler, G.; Feeney, J.; Roberts, G. C.; Benkovic, S. J. Biochemistry 1989, 28, 5743-5750
58. Bell, R. P. The tunnel effect in chemistry; Chapman & Hall: London & New York, 1980.
59. Kohen, A.; Klinman, J. P. Acc. Chem. Res. 1998, 31, 397-404
60. Kohen, A.; Klinman, J. P. Chem. Biol. 1999, 6, R191-198
61. Meyer, M. J.; Tomchick, D. R.; Klinman, J. P. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 1146
62. Hay, S.; Sutcliffe, M. J.; Scrutton, N. S. Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 507-512
63. Kamerlin, S. C. L.; Mavri, J.; Warshel, A. FEBS Lett. 2010, 584, 2759-2766
64. Khavrutskii, I. V.; Price, D. J.; Lee, J.; Brooks, C. L. I. Protein Sci. 2007, 16, 1087-1100
65. Mesecar, A. D.; Stoddard, B. L.; Koshland, D. E. Science 1997, 227, 202-206
66. Garcia-Viloca, M.; Truhlar, D. G.; Gao, J. Biochemistry 2003, 42, 13558-13575
67. Sawaya, M. R.; Kraut, J. Biochemistry 1997, 36, 586-603